1. THE ROLE OF NATURAL FACTORS IN THE LIMITATION OF OF PREY NUMBERS: A BRIEF REVIEW OF THE EVIDENCE Ian Newton

Summary 1. populations are normally limited, rather than fluctuating at random. In the absence of human intervention, the limitation in many comes through competition for breeding space, and is helped by the presence of surplus adults, which breed only when an existing nesting territory becomes vacant. 2. In where nest sites are freely available, breeding density is often limited by food supply. This may be inferred from the following findings: (a) species that exploit fairly stable (often varied) food sources show fairly stable densities, which differ between regions where food abundance differs; (b) species that exploit annually fluctuating (often restricted) food supplies show fluctuating densities; and (c) species that are exposed to a long-term or step-wise change in food supply show a long term or step-wise change in density. In other areas, however, breeding density may be restricted by shortage of nest sites to a lower level than would normally occur with the available food-supply. This may be inferred from: (a) the absence of breeding pairs in areas that lack nest sites but are otherwise apparently suitable; (b) the provision of artificial nest sites is sometimes followed by a big increase in breeding density; and (c) the loss of nest sites is sometimes accompanied by a decline in breeding density. Hence, in the available in any one region, breeding density is naturally limited by food supply or nest sites, whichever is most restricting. 3. As a consequence of persecution (past or present) or other human actions, many modern populations are below the level that would be permitted by the habitat. Some species may also be limited in numbers and distribution by other of prey, which eat them or compete for food or nest-sites. 4. Aspects in need of further study include: (a) effects of widescale food manipulation experiments on population density and individual behaviour; (b) behavioural mechanisms that lead birds to adjust their spacing (and density) to prevailing food-supply; (d) effects of interactions (competitive or predatory) between different predator species on raptor and owl breeding densities; and (d) movements of nomadic species between successive nesting areas, best done by the satellite- tracking of radio-tagged individuals.

1.1 Introduction Although raptor populations over much of the world have been reduced by human activities - by habitat destruction, deliberate persecution, and by and other toxic

5 Birds of Prey in a Changing Environment chemicals - enough studies of intact populations have now been made to suggest how densities are naturally limited. In this chapter I shall be concerned primarily with the natural limitation of breeding density in birds of prey and only peripherally with human impacts. The chapter is intended as a scene setter, and the approach is comparative; it is partly an update of earlier reviews (Newton, 1979, 1991a,b), focussing on more recent research, but also draws on studies of owls (Strigiformes) as well as those of diurnal raptors ().

1.2 Evidence that densities are regulated For some raptor species, the idea that breeding density is regulated, rather than fluctuating at random, is based on four main findings: (1) the stability of the breeding populations of many species, in both size and distribution, over periods of many years; (2) the existence of surplus adults, physiologically capable of breeding, but attempting to do so only when a territory is made available through the death or removal of a previous occupant; (3) the re- establishment of populations, after their removal by man, to the same level as previously; and (4) in areas where nest sites are not restricted, in many species a regular spacing of breeding pairs. In the sections below, these points are examined in turn.

1.2.1 Stability of breeding population Some raptor species show some of the most stable breeding densities known among birds, as can be documented from long-term studies (Newton, 1979, 1991b). An example is the golden eagle Aquila chrysaetos in which the density of territorial pairs in some sizeable areas may vary by no more than 15% of the mean level over periods up to several decades (Newton, 1979; Watson, 1996; Steenhof et al., 1997). Compared to findings on others birds (Lack, 1954, 1966), and to what is theoretically possible, this represents a remarkable degree of stability. Similar evidence for such relative stability over fewer years is available for at least a dozen other raptor species in various parts of the world (Newton, 1979). Evidence for long-term stability also comes from studies of the total raptor fauna of particular areas. Near Berlin, Wendland (1952-53) found constancy in the numbers of individual species, and hence of the raptor population as a whole, over an 11 year period. Craighead & Craighead (1956) obtained similar results in three study years covering a seven-year period in Michigan. Stability of breeding densities, as shown in the above studies, would be expected only in stable environments. It would not be expected in habitats that were changing rapidly through vegetation succession or human action, or in which prey densities were changing. Nor would it be expected in those populations recovering from past persecution or impacts. In practice, the degree of variability in any bird population tends to increase with the span of years over which counts are made (Newton, 1998). This is partly because the chance of including an unusual year increases with the length of study, and also because the year-to-year fluctuations may be superimposed on a long-term upward or downward trend. In fact, wherever bird species have been studied over periods of several decades, their abundance and distribution patterns are often found to have changed greatly. Peregrines in Britain provide a well-documented example, for even in regions where they have not previously been heavily persecuted, they are much more numerous now than 70 years ago (Ratcliffe, Chapter 4).

6 The role of natural factors in the limitation of bird of prey numbers

1.2.2 Surplus birds In some populations, non-breeding, non-territorial adults can be seen near nest sites, occasionally fighting with breeders, and even killing and replacing them (Gargett, 1975; Monneret, 1988; Bowman et al., 1995, Haller, 1996). However, the main evidence for the existence of surplus birds, which breed only when a place becomes available, is that lost mates are often replaced in the same season by other individuals, which then breed themselves. Replacement sometimes occurs within a few days, and is evidently widespread among raptors. Specific instances, reported incidentally in the literature, involve at least 26 species, from small to large vultures, and include both solitary and colonial species (Newton, 1979). At some nest sites, more than one replacement was recorded (where shooting was continued), and at other sites individuals of both sexes were replaced. Most instances referred to females, perhaps because they were more easily shot than males, or because they were more numerous among surplus birds. Replacements included some birds in adult plumage and others in immature plumage. Documented instances were mainly from the early literature and, as evidence for the existence of surplus birds, were often equivocal. In recent years, properly controlled removal experiments, of the kind done on other birds, have been conducted on at least three species of raptors, namely the common Falco tinnunculus, the Falco sparverius and the Accipiter nisus (Table 1.1; Village, 1983; Bowman & Bird, 1986; Newton & Marquiss, 1991). In all of these species, replacement of removed individuals occurred, sometimes within days, indicating the presence of surplus birds of both sexes, mostly in the younger age groups, capable of breeding when a vacancy appeared. In each case, birds from neighbouring territories were marked, so it could be shown that the replacement individuals had not simply moved from other territories nearby.

Table 1.1. Results of experimental removal of breeders from nesting territories in early spring (pre-laying). Details from Newton & Marquis (1991), Village (1983) and Bowman & Bird (1986).

Sparrowhawk Kestrel American kestrel

Male Female Male Female Male Female

Number removed 7 7 10 11 16 4 Number replaced 3 3 3 7 8 1 Number produced eggs 1 3 2 7 4 Number produced young 0 1 0 6 ?

Few attempts have been made to estimate the numbers of floaters in raptor populations. However, Newton & Rothery (2001) calculated that at least 22% of female sparrowhawks present at the start of the breeding season were floaters. From radio-tracking data, Kenward et al. (1999, 2000) calculated the proportion of non-breeders in a population in spring at 75% or more, and in a goshawk population at 29% of males and 60% of females (which had higher survival than males), but these latter estimates included territorial non-breeders, as well as floaters. All three populations were judged to be close to the level that the habitat could support, and in depleted or expanding populations the expected proportions of floaters would be lower.

7 Birds of Prey in a Changing Environment

1.2.3 Re-establishment of populations In Britain, instances are known of local breeding populations being removed or depleted by human action, and then recolonizing or recovering to about the same level as previously, with pairs in the same nesting places. This occurred with peregrine falcons Falco peregrinus shot during 1939-45 on the south coast of , and depleted by pesticide poisoning during the 1960s in many other regions (Ratcliffe, 1993). In each case, not only did the newcomers use the same cliffs as their predecessors, but also the same nest ledges. One of the most remarkable examples involved the merlin Falco columbarius (Rowan, 1921-22), in which four or five pairs of this small settled each year on an area of the North York Moors in eastern England. For more than 20 consecutive years, all of the pairs were shot and no young were raised. Yet each year four or five new pairs settled in the same places as their predecessors. Such events imply constancy in the carrying capacity of the environment over the years, with the same limitations on breeding numbers. Again this would be expected only in landscapes that remained reasonably stable over the years, and not in those altered by human action. In some parts of Britain, peregrines now breed at greater density than previously, but this has been attributed to increase in their food supply in the form of racing pigeons (Crick & Ratcliffe, 1995).

1.2.4 Regular spacing In continuously suitable nesting habitats, a regular spacing of breeding pairs has been documented in many kinds of raptors and owls, and is evidently widespread in solitary nesting species (for common buzzard, see Tubbs, 1974; for golden eagle Aquila chrysaetos, see Watson, 1996; for peregrine falcon, see Ratcliffe, 1993; for sparrowhawk, see Newton et al., 1977, 1986; for tawny owl Strix aluco, see Southern, 1970). Such spacing, reflecting the territorial behaviour of individual pairs, is consistent with the idea of density limitation, especially when the same pattern holds over many years. It would not, of course, be expected where nest sites were sparse and irregular in distribution, constraining the distribution of breeding pairs. These four arguments, taken together, provide circumstantial evidence that: (a) breeding density is limited, (b) the limitation results from competition for breeding space (or ‘territories’); and (c) stability of breeding density is helped by the existence of surplus birds, encouraged to breed only when a territory is vacated and a gap is made available. We should not assume that surplus birds are available at all times in all populations; or that all non- breeders are capable of breeding that year if a place were made available to them. In species in which individuals do not breed until they are several years old, many birds in the non- territorial sector are likely to be immature, and perhaps unable to defend a territory, let alone breed. In many studies of fairly stable populations, in each year some previous territories remained vacant. The usual occupancy of British peregrine territories pre-1939 was 85% (Ratcliffe, 1972), and in some common buzzard territories it was 77-83% (Tubbs, 1974). Territories vary in quality - that is in the opportunities they offer for survival and successful breeding - and possibly some poor territories are suitable for occupation only in certain years, or only by certain birds (Newton, 1988). In the removal experiments on sparrowhawks reported above, birds taken from known good territories were quickly replaced, while those taken from known poor territories nearby were not. Also, when given

8 The role of natural factors in the limitation of bird of prey numbers the opportunity to breed, replacement birds bred much less well than other first-time settlers. This was especially true of males. Findings from raptors thus underline the importance of both site features and bird features in influencing whether settlement, defence and breeding occur.

1.2.5 Regulation of breeding density around a constant level Research on sparrowhawks in south Scotland revealed how breeding density was regulated around a constant level over a 20 year period. In this 200 km2 area, nest numbers fluctuated from year to year but remained throughout within 15% of the mean level, with no long- term upward or downward trend. Each year almost all of the breeding females were trapped for ringing and identification, so each year the new breeders could be separated from the established ones remaining from previous years. In general, the numbers of new breeders added each year matched the numbers of older ones lost from the previous year (Figure 1.1). In this way, long-term stability of the population was maintained by density-dependent recruitment (Newton, 1991a). Such a regulatory system can operate only while there are enough floaters to fill the gaps, otherwise breeding numbers would decline.

Figure 1.1. Density-dependent recruitment to a breeding population of the Eurasian sparrowhawk, south Scotland, 1975-89. The breeding population remained fairly stable during this period, and the numbers of new breeders recruited each year (y) were inversely related to the numbers of established breeders remaining from the previous year (x). Regression relationship: y = 31.7-0.90x, r=0.69, N=14, P<0.003. Population stability was itself a consequence of a fairly stable territorial system, in which the landscape was apparently occupied to a similar level each year. From Newton (1991).

9 Birds of Prey in a Changing Environment

1.3 Density limitation in relation to food supplies In the limitation of breeding numbers within suitable habitat, two resources seem of major importance to birds of prey, namely food supplies and nest sites (Newton, 1979). Consider first the relationship between breeding densities and food supplies in areas where nest sites are freely available.

1.3.1 Regional variations in breeding density In some species, regional variations in breeding density are associated with regional variations in prey supplies. Sparrowhawk nesting densities in the woods of 12 different regions of Britain varied in relation to the local densities of prey birds. The hawks nested closer together, at higher densities, in areas where their prey were most numerous. The woods in all of these areas were of roughly similar structure, and the differences in prey densities were associated with variation in elevation and soil type (Newton et al., 1977, 1986). Similar relationships between regional breeding densities and prey densities have been documented for common kestrel (Village, 1990), common buzzard (Newton, 1979; Graham et al., 1995), golden eagle (Watson et al., 1992) and peregrine in Britain (Ratcliffe, 1969), and in these and other species elsewhere. In solitary nesting raptors the link between density and food supply is apparently brought about by spacing behaviour, as birds adjust their spacing (territory sizes) to correspond with the food situation. In permanent residents, such as golden eagles in Scotland, density is most closely related to food supply (carrion) in winter when food is scarcest (Watson et al., 1992), but in summer migrants, such as in Scotland, it is adjusted to food supply in spring, at the time of settling (Village, 1990). Unusually high densities of raptors are invariably associated with an unusual abundance of food. Examples of natural situations are the abundance of peregrines around large seabird colonies (Beebe, 1960), of ospreys Pandion haliaetus around fisheries (Henny, 1988), and of black eagles Aquila verreauxii around hyrax concentrations (Gargett, 1975), but even greater densities of raptors occur in some African and Asian cities, where human activity provides the food. The city of Delhi, in , covers 150 km2 and in 1967 held an estimated 2,900 raptor pairs, a density of more than 19 pairs per km2(Galushin, 1974). These were mainly scavenging species, such as black kite Milvus migrans (15 pairs per km2) and white-backed vulture Gyps africanus (four pairs per km2), but also included some other species. This high density was associated primarily with a huge amount of food within the city (mainly garbage and carcasses), but also with an abundance of nesting sites, and an unusual tolerance by the human population. The implications from such natural variation are that raptors respond to the food situation, and that solitary species space themselves more widely, in larger territories, where food is sparse. An earlier argument, on whether food or behaviour limits density, becomes redundant if the birds adjust the spacing to the resources available (Marquiss & Newton, 1982; Village, 1983). So one line of evidence that breeding density is limited in relation to food supply comes from the long-term stability of populations, but at different densities in different regions.

1.3.2 Annual variations in breeding density For other species, the idea that breeding density is adjusted in relation to food supply comes not from long-term stability in density, but from annual fluctuations in density which

10 The role of natural factors in the limitation of bird of prey numbers parallel fluctuations in food. Most species in the regions concerned have restricted diets based on cyclic prey. Two main cycles are recognised: (a) an approximate four-year cycle of on northern tundras, boreal forests and temperate grasslands; and (b) an approximate ten-year cycle of snowshoe hares Lepus americanus in the boreal forests of . Some gamebirds are also cyclic, but whereas in northern they follow the four-year cycle, in North America they follow the ten-year hare cycle (Lack, 1954; Keith, 1963). The main raptor and owl species that depend on such prey show great year-to-year fluctuation in breeding density in parallel with fluctuation in their food supply (Table 1.2). Moreover, some species, such as the , fluctuate in density where they feed on cyclic prey, but remain fairly stable in density where their food- supply is more stable (often through being more varied). Such regional variation within species provides further circumstantial evidence for a link between breeding density and food supply.

Table 1.2. Annual variation in breeding numbers of raptors and owls that exploit greatly fluctuating food sources.

Species that eat rodents (approximately 4 year cycles)

Rough-legged hawk Buteo lagopus • 0-9 pairs during 9 years, North Norway (Hagen, 1969)* • 26-90 pairs during 34 years, Colville River, Alaska (Mindell et al., 1987) • 10-82 pairs during 5 years, Seward Peninsula, Alaska (Swartz et al., 1974) • 0-27 pairs during 6 years, NW Territories (Court et al., 1988)

Hen harrier Circus cyaneus • 10-24 females in 33 km2 during 22 years, Orkney, Scotland (Balfour, in Hamerström, 1969) • 13-25 females in 160 km2 during 5 years, Wisconsin (Hamerström, 1969)*† • 0-9 pairs in 6 years between 1938 and 1946 (Hagen, 1969)* • 8-22 pairs during 8 years, Scotland (Redpath et al., 2002)*

Common kestrel Falco tinnunculus • 35-109 clutches during 4 years; Netherlands (Cavé, 1968)* •Approximately 20-fold fluctuation in index of number of broods ringed in Britain over 42 years, with peaks every 4-5 years (Snow, 1968)* • 1-14 pairs during 5 years, North Norway (Hagen, 1969)* • 1-16 nests during 12 years, Swabian Alps (Rockenbauch, 1968)* • 28-38 pairs during 4 years, south Scotland, 9-28 pairs and 12-22 pairs in two areas during 6 years, southern England (Village, 1990)* • 2-46 pairs during 11 years, western Finland (Korpimäki & Norrdahl, 1991)* • 2-29 pairs during 23 years, northern England (Petty et al., 2000)*

Black-shouldered kite Elanus axillaris •Increase from 1 to 8 nests in one year, associated with rodent plague, South (Malherbe, 1963)* • 19-35 individuals, during 3 years, Transvaal, South Africa (Mendelsohn, 1983)*

11 Birds of Prey in a Changing Environment

Long-eared owl Asio otus • 1-19 pairs during 11 years, western Finland (Korpimäki & Norrdahl, 1991)* • 9-18 pairs during 4 years, south Scotland (Village, 1981)*

Short-eared owl Asio flammeus • 0-28 pairs during 2 years, northern Alaska (Pitelka et al., 1955)* • 0-49 pairs during 11 years, western Finland (Korpimäki & Norrdahl, 1991)* • 0-27 pairs (index) during 23 years, northern England (Petty et al., 2000)*

Snowy owl Nyctea scandiaca •3 and 7 pairs during 2 years, northern Alaska (Pitelka et al., 1955)*

Tengmalm’s owl Aegolius funereus • 3-63 pairs during 7 years, western Finland (Korpimäki, 1985)*

Barn owl Tyto alba • 14-94 pairs during 13 years, south Scotland (Taylor, 1994)*

Species that eat gallinaceous birds and rabbits (4-year or 10-year cycles)

Ferruginous hawk Buteo regalis • 5-16 pairs during 8 years in one area, 1-8 pairs during 3 years in another area, Utah (Woffinden & Murphy, 1977)*

Northern goshawk Accipiter gentilis • 0-4 nests during 13 years; 2-9 nests during 7 years, in two areas of Sweden (Höglund, 1964) • 1-9 nests during 4 years, Alaska (McGowan, 1975) • 0-11 pairs during 7 years, Yukon (Doyle & Smith, 1994)* • 11-28 pairs during 13 years, Finland (Wikman & Lindén, 1981)*

Gyr falcon Falco rusticolus • 13-49 pairs during 5 years, Seward Peninsula, Alaska (Swartz et al., 1974)* • 19-31 occupied cliffs and 12-29 successful nests during 4 years, Alaska (Platt, 1977)* • 8-19 pairs during 27 years, Colville River, Alaska (Mindell et al., 1987) • 19-31 pairs during 4 years, Brooks Range, Alaska (Platt, 1977) • 39-63 occupied territories during 17 years, north-east Iceland (Nielsen, 1999)*

Great horned owl Bubo virginianus • 20-40 territory holders, 20-86 total birds during 6 years, Yukon (Rohner, 1995)*

*Prey population also assessed and related to raptor numbers. † Excluding one year when population dropped from DDT poisoning.

Populations of microtine rodents do not reach a peak simultaneously over their whole range, but the cycles may be synchronised over tens, hundreds or many thousands of square kilometres, out of phase with those in more distant areas. However, peak populations may

12 The role of natural factors in the limitation of bird of prey numbers occur simultaneously over many more areas in some years than in others, giving a measure of synchrony, for example, to lemming cycles over large parts of northern Canada, with few regional exceptions (Chitty, 1950). In addition, the periodicity of cycles tends to increase northwards, from about three years between peaks in temperate and southern boreal regions, increasing to four or five years in northern boreal regions. The amplitude of the cycles also increases northwards from barely discernible cycles in some temperate regions to marked fluctuations further north, where peak densities typically exceed troughs by more than a hundred-fold (Hanski et al., 1991). Even further north, on the tundra, the periodicity of lemming cycles is in some places even longer (five to seven years between peaks on Wrangel Island (Menyushina, 1997)), and the amplitude is even greater, with peaks sometimes exceeding troughs by more than a thousand-fold (Shelford, 1945). In most places, the increase phase of the cycle usually takes two to three years, and the crash phase one to two years. Importantly, the crash phase often overlaps with spring and summer, a time when rodent predators are breeding. The longer hare cycles have been less extensively studied, but peaks in numbers can exceed troughs by more than a hundred-fold (Adamcik et al., 1978). Unlike the situation in rodents, the cycle is more or less synchronised over much of boreal North America, with populations across the continent peaking in the same years (Keith & Rusch, 1988). Raptors and owls show two main types of response to cyclic fluctuations in their food- supply (Figure 1.2). One type is shown by resident species, which tend to stay on the same territories year-round and from year to year. While preferring rodents (or lagomorphs), they eat other prey, so they can remain in the same area through low rodent years. However, their survival may be poorer, and their productivity much poorer, in low than in high prey years. In low prey years, the majority of territorial pairs may make no attempt to breed, and those that do, lay relatively small clutches and raise small broods. The common buzzard, tawny owl, Strix uralensis, barn owl Tyto alba and great horned owl Bubo virginianus are in this category, responding functionally to prey numbers, and numerically chiefly in terms of the numbers of young raised (Mebs, 1964; Southern, 1970; Saurola, 1989; Petty, 1992; Taylor, 1994; Rohner, 1996). This type of response, shown by resident populations, produces a lag between prey and predator numbers, so that high predator densities follow good food-supplies and low densities follow poor supplies (Figure 1.2). Prey and predator densities fluctuate in parallel, but with the predator behind the prey (up to two years behind in the snowshoe hare-great horned owl system (Rohner, 1995)). The lag period depends partly on the age at which first-breeding in the predator occurs. In the tawny owl, young produced in a peak vole year often breed in the following year, just before vole numbers crash (Petty, 1992), but in the great horned owl most individuals reach two or more years before they attempt to breed (Rohner, 1995)). The same holds for gyr falcons Falco rusticolus in Iceland, where the main prey species (rock ptarmigan Lagopus mutus) fluctuates with roughly ten-year periodicity and where the total numbers of falcons showed a two year lag, and the numbers of territorial falcons a three year lag, behind the peak ptarmigan year (Nielsen, 1999, Chapter 24). The second type of response is shown by ‘prey-specialist’ nomadic species, which concentrate to breed in different areas in different years, depending on where their food is plentiful at the time. Typically, individuals might have one to two years in the same area in each three to five year vole cycle, before moving on when prey decline. They thus respond

13 Birds of Prey in a Changing Environment

a)

b)

c)

Figure 1.2. Fluctuations in the numbers of breeding and non-breeding owls in relation to indices of vole densities. (a) Short-eared owl, immediate response; (b) barn owl, lag in response in decline years; (c) great horned owl, long lag in response, with the peak in total owl numbers one year behind the peak in prey numbers, and in breeding owl numbers two years behind. From Korpimäki & Norrdahl (1991), Taylor (1994), and Rohner (1995). to their food supplies more or less immediately, so that their local densities can match food supplies at the time, with minimal lag. Familiar examples from among owls include the short-eared owl Asio flammeus, long-eared owl Asio otus, northern hawk owl Surnia ulula, and to some extent, snowy owl Nyctea scandiaca and great grey owl Strix nebulosa, and from among raptors the rough-legged buzzard Buteo lagopus and in some areas the common kestrel, hen harrier Circus cyaneus, Montagu’s harrier Circus pygargus and black-winged kite Elanus caeruleus (Table 1.2). The local densities of most such species can vary from nil in low rodent years to several tens of pairs per 100 km2 in intermediate (increasing) or high rodent years. In an area of

14 The role of natural factors in the limitation of bird of prey numbers western Finland, for example, over an 11 year period, numbers of short-eared owls varied between 0 and 49 pairs, numbers of long-eared owls between 0 and 19 pairs, and numbers of kestrels between 2 and 46 pairs, in accordance with spring densities of Microtus (Korpimäki & Norrdahl, 1991). When voles are plentiful, such species tend to raise large broods, so if they are successful in finding prey-rich areas year after year, individuals could in theory breed well every year, buffered from effects of local fluctuations in their prey. In practice, however, they may not always find suitable prey-rich areas. In all of the owl species mentioned, individuals have sometimes been seen in areas with low prey populations, typically as single wide-ranging non-breeders, rather than as territorial pairs (e.g. Pitelka et al., 1955; Menyushina, 1997). In addition, if previously high rodent numbers crash during the course of a breeding season, nest desertion and chick mortality can be high. Under these conditions, 22 out of 24 nests of short-eared owls in south Scotland failed, and most of the adults left the area in early summer, when they would normally be raising young (Lockie, 1955). Relationships between nomadic owl and microtine densities have been studied mainly in particular areas, monitored over a number of years. Such studies have revealed temporal correlations between predator and prey numbers. However, spatial correlations were found by Wiklund et al. (1998), who counted predators and prey in 15 different localities on the Eurasian tundra in a single year. These areas extended from the Kola peninsula in the west, through 140° of longitude, to Wrangel Island in the east. Comparing areas, densities of snowy owl (and two skua Stercorarius species) were correlated with densities of lemming, which were at different stages of their cycle in different areas. The two responses (delayed and simultaneous) are not completely distinct, and different species of owl and raptor may be better described as showing a graded response, from the most sedentary at one end to the most mobile at the other. Moreover, the same species may show regional variation in behaviour depending on food supply, and the extent to which alternative prey are available when favoured prey are scarce. The more varied the diet, the less the chance of all prey types being scarce at the same time. Korpimäki (1986) examined the population fluctuations, movements and diet of Tengmalm’s owls Aegolius funereus from studies at 30 different European localities extending from about 50°N to 70°N. The amplitude and cyclicity of owl population fluctuations increased northwards, while diet breadth and degree of site fidelity decreased northwards. This fitted the fact that microtine fluctuations became more pronounced and more synchronised northwards, while the number of alternative prey decreased. Furthermore, snow conditions were more important in the north, because this small owl cannot easily get at voles under deep snow. According to Korpimäki (1986), then, Tengmalm’s owl could be described as a resident generalist predator of small and birds in central Europe, as partially nomadic (with males resident and females moving around) in south and west Finland, and as a highly nomadic microtine specialist in northern Fennoscandia, in areas with the most pronounced vole cycles. Among lagomorph feeders, the great horned owl and goshawk seem to show much greater fluctuation in breeding density in the north of their North American range, where they depend primarily on snowshoe hares, than further south where they have a wider range of prey, but I know of no detailed studies in the southern parts. There would be little value in great horned owls or goshawks in northern areas breeding nomadically, because, as mentioned above, snowshoe hares seem to fluctuate in synchrony over their whole range.

15 Birds of Prey in a Changing Environment

Birds leaving one area because of a shortage of hares would be unlikely to find many more hares anywhere else. This is in marked contrast to the situation in microtine-feeding species.

1.3.3 Long-term or step-wise changes in food supplies Some raptor species, which are normally fairly stable in numbers, have shown a marked change in breeding density following a marked change in food supply. Often such population changes result from human impacts on habitats, but not always. An example is provided by the buzzard in Britain, in which breeding densities fell after the viral disease myxomatosis reduced the number of rabbits that formed the main prey. In one area, numbers dropped from 21 pairs to 14 pairs between one year and the next, as rabbit numbers were reduced (Dare, 1961). Lest anyone think from the foregoing that marked temporal changes in breeding density occur only in species that eat microtines or lagomorphs, consider the peregrine. In parts of Britain nesting densities have increased greatly in recent decades (to well above any previously recorded levels), in association with the increased availability of homing pigeons, a favourite prey (Ratcliffe, 1993; Crick & Ratcliffe, 1995).

1.3.4 Modifying influence of weather In much of northern and North America, winter snow provides a protective blanket over small rodents that live and breed in the vegetation beneath. The level of protection that snow provides depends on its depth, the hardness of the surface crust and the duration of lie, all of which tend to increase with latitude. Different species of rodent-eating raptors and owls vary in their ability to detect and secure rodents under snow, and in general the larger (heavier) species are better able to penetrate snow than smaller ones. The great grey owl is renowned for its ability to smash through hard deep snow (45 cm or more) to catch rodents which it apparently detects by ear (Nero, 1980), while small species, such as Tengmalm’s owl, are disadvantaged by even very shallow snow (Sonerud, 1984). The behaviour of the rodents themselves also affects their accessibility to their avian predators, particularly the frequency with which they emerge and run along the surface. Prolonged snow cover can sometimes stop rodent-eaters from responding in the usual way to a rodent peak in early spring, affecting breeding density, proportion of pairs nesting and clutch sizes (for snowy owl, see Menyushina, 1997), and in some winters it can lead to large-scale starvation even when voles are plentiful (for barn owl, see Shawyer, 1987; Taylor 1994; and for tawny owl, see Jedrzejewski & Jedrzejewski, 1998; Saurola, 1997). In some areas, year-to-year changes in resident breeding populations of common kestrel have been linked with winter weather, which influences food availability (Village, 1990; Kostrzewa & Kostrzewa, 1991). Marked declines in kestrel numbers, associated with heavy mortality, occur in years of prolonged snow cover, when rodents remain hidden for long periods. Larger species, which can withstand longer periods on reduced rations, seem much less affected by hard winters.

1.4 Density limitation in relation to nest sites In some districts, bird of prey breeding densities are held by shortage of nest sites below the level that the available food supply would be expected to support. The evidence is of two kinds: (a) breeding raptors are scarce or absent in areas in which nesting places are scarce or

16 The role of natural factors in the limitation of bird of prey numbers absent, but which otherwise appear suitable (non-breeders may live in such areas); and (b) the provision of artificial nest sites is sometimes followed by an increase in breeding density, while removal of nest sites can lead to a decrease in breeding density. Kestrel numbers increased from a few pairs to more than 100 pairs when nesting boxes were provided in a Dutch polder area with few natural sites (Cavé, 1968). Similar results were obtained with other populations of kestrel, and also with American kestrels, ospreys and prairie falcons Falco mexicanus (Reese, 1970; Rhodes, 1972; Hamerström et al., 1973; R. Fife, pers. comm.). Among owls, increases in breeding density following nest site provision have been noted in little owls Athene noctua, barn owls, Ural owls and others (Mikkola, 1983; Exo, 1992; Petty et al., 1994). The results from a controlled experiment on common kestrel are given in Table 1.3.

Table 1.3. Results of experimental provision of nest sites for European kestrels in areas previously devoid of breeding kestrels. All birds used the boxes provided and included both first year and adult breeders. From Village (1983).

No. of nest No. of pairs nesting sites provided in same year

Experimental areas 17 8 Control areas 0 0

Sometimes the provision of nesting sites has facilitated an extension of breeding range, as exemplified by the Mississippi kite Ictinia mississippiensis and other species which nest in tree plantations on North American grasslands (Parker, 1974). Likewise, nesting on buildings has allowed peregrines and other cliff nesters to breed in areas otherwise closed to them through lack of nest sites. On the other hand, the destruction of nesting sites has sometimes led to reductions in breeding density, as in certain eagles when large free- standing trees were felled (Bijleveld, 1974), in peregrines when cliffs providing nest sites were destroyed by mining (Porter & White, 1973) and in barn owls when old buildings were demolished or renovated (Taylor & Walton, Chapter 32). In addition, when nest sites are scarce, species may compete for them, and the presence of one dominant species may restrict the numbers and distribution of another (Newton, 1979).

1.5 Winter densities Some raptors stay on their breeding sites all year, but others spread over a wider area after breeding, or migrate to a completely different area. Outside of the breeding season, nest sites are less important, so in theory the birds have greater freedom to move around, and can exploit temporary food sources in a way not possible while breeding. Some Palaearctic raptors, which winter in Africa, may spend most of their time between breeding seasons on the move, following rain belts, and exploiting temporary abundances of , locusts, and other prey (Newton, 1979). At this season, therefore, food can take over as the all- important limiting factor. The few studies that have been made of species that remain in an area all winter again imply that food supply has a major influence on density. For example, Craighead & Craighead (1956) compared the raptor population in an area of Michigan over two years, in one of which there was a high vole population and in the other a low one. In the good vole year, 96 raptors of seven species were present in the area, but in the poor year only 27

17 Birds of Prey in a Changing Environment individuals of five species were counted. Other studies involve individual species over longer periods (e.g. Village, 1990). Evidently, within the habitats that are occupied, food supply can be an important limiting factor at all seasons.

1.6 Discussion 1.6.1 Food and nest sites To judge from available evidence, the carrying capacity of any habitat for raptors and owls is set by two main resources, food and nest sites, and whichever is most restricted is likely to limit breeding density. On this basis, much of the natural variation in breeding densities can probably be explained. However, much of the relevant research has been done on resident populations, and it is possible that some migrant populations may be limited on winter quarters, and so be unable to occupy their breeding habitat to the full. The European honey buzzard Pernis apivorus provides a possible example. This situation is analogous to that of some small resident species which, at mid-to-high latitudes are in some years reduced by winter severity below the level that nesting habitat would support. Most of the evidence presented above on the role of food and nest sites is based on correlations, but experiments have confirmed the existence of surplus birds in some populations, and the provision of nest sites has confirmed their importance as potential limiting factors. So far, to my knowledge, no proper experiments have been made that involve manipulation of the food supply of whole populations (as opposed to individuals). This is an obvious gap in the study of raptor populations, the results of which could have applications in management; for however good a habitat in other respects, raptors cannot occupy it without the prey to support them. Another aspect in need of further study concerns the precise mechanism which leads individuals to take larger territories (giving lower densities) where food is scarce. Do territory owners have to forage more widely in such conditions, simply extending their defence accordingly and ‘forcing out’ their weaker neighbours; or are owners obliged to take smaller territories in areas of high food density because the many birds attracted to such areas push up the defence costs of large territories to unsustainable levels (Temeles, 1987; Newton, 1998, pp. 46-48)? These are only two of several possible mechanisms, and food provision experiments, together with observations on marked birds, might help to decide between them. In the so-called ‘nomadic’ rodent-eating species, which concentrate to breed in widely separated areas in different years, little is known of how individuals find prey-rich areas, or of how far they move between breeding seasons. Although some revealing ring recoveries are available (see Newton, 2002, for owls), such questions would be better addressed by use of satellite tracking of radio-tagged individuals.

1.6.2 Other limiting factors Food and nest sites are, of course, not the only factors limiting the current numbers and distributions of raptors in Britain and elsewhere. Many populations are held by persecution (past or present), or by pesticides and other toxic chemicals, below the level that the contemporary landscape would support. In addition, most raptor populations in Britain are currently in the process of change, either in recovery from past persecution or pesticide impacts, or in decline from renewed persecution or habitat degradation and decline in food-

18 The role of natural factors in the limitation of bird of prey numbers supplies. Nonetheless, study of the natural limiting factors, as discussed above, provides a useful framework within which to organise our thinking and to plan our management efforts. A largely unexplored aspect is the extent to which the numbers and distributions of some raptor and owl species may be limited by the presence of other species. Such limitation could occur either through competition for a shared food supply, by direct predation of small species by large ones, or by small species avoiding large ones, and thereby having less habitat or fewer nest sites available to them. Such matters are likely to require more attention in Britain as goshawks extend their range, with potential effects on smaller raptors and owls, and if eagle owls establish themselves (nesting recorded in at least three widely separated areas in recent years). Both these species include many smaller raptors in their diets, and could influence their population levels. Instances are on record of golden eagles displacing peregrines from cliff nest-sites, and peregrines displacing kestrels (Newton, 1979). In addition, some owl species have been suspected of limiting the distribution of others (for Eurasian eagle owl possibly affecting Ural owl, see Saurola (1992); for Ural owl possibly affecting Tengmalm’s owl, see Hakkarainen & Korpimäki (1996); for tawny owl possibly affecting Tengmalm’s and Eurasian pygmy owls, see Koenig (1998); and for Ural owl and tawny owl possibly affecting one another, see Lundberg (1980)). It is clear, therefore, that while food supply is the primary limiting factor for many raptors and owls, nest site shortages, adverse weather or other secondary factors can sometimes reduce breeding densities and performance substantially below what the food supply would otherwise permit.

Acknowledgements I am grateful to two anonymous referees for helpful comments.

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24